Auswahl der wissenschaftlichen Literatur zum Thema „Transition monoderme/diderme“

The very nature of the last bacterial common ancestor (LBCA), in particular the characteristics of its cell wall, is a critical issue to understand the evolution of life on earth. Although knowledge of the relationships between bacterial phyla has made progress with the advent of phylogenomics, many questions remain, including on the appearance or disappearance of the outer membrane of diderm bacteria (also called Gram-negative bacteria). The phylogenetic transition between monoderm (Gram-positive bacteria) and diderm bacteria, and the associated peptidoglycan expansion or reduction, requires clarification. Herein, using a phylogenomic tree of cultivated and characterized bacteria as an evolutionary framework and a literature review of their cell-wall characteristics, we used Bayesian ancestral state reconstruction to infer the cell-wall architecture of the LBCA. With the same phylogenomic tree, we further revisited the evolution of the division and cell-wall synthesis (dcw) gene cluster using homology- and model-based methods. Finally, extensive similarity searches were carried out to determine the phylogenetic distribution of the genes involved with the biosynthesis of the outer membrane in diderm bacteria. Quite unexpectedly, our analyses suggest that all cultivated and characterized bacteria might have evolved from a common ancestor with a monoderm cell-wall architecture. If true, this would indicate that the appearance of the outer membrane was not a unique event and that selective forces have led to the repeated adoption of such an architecture. Due to the lack of phenotypic information, our methodology cannot be applied to all extant bacteria. Consequently, our conclusion might change once enough information is made available to allow the use of an even more diverse organism selection.

One of the major unanswered questions in evolutionary biology is when and how the transition between diderm (two membranes) and monoderm (one membrane) cell envelopes occurred in Bacteria. The Negativicutes and the Halanaerobiales belong to the classically monoderm Firmicutes, but possess outer membranes with lipopolysaccharide (LPS-OM). Here, we show that they form two phylogenetically distinct lineages, each close to different monoderm relatives. In contrast, their core LPS biosynthesis enzymes were inherited vertically, as in the majority of bacterial phyla. Finally, annotation of key OM systems in the Halanaerobiales and the Negativicutes shows a puzzling combination of monoderm and diderm features. Together, these results support the hypothesis that the LPS-OMs of Negativicutes and Halanaerobiales are remnants of an ancient diderm cell envelope that was present in the ancestor of the Firmicutes, and that the monoderm phenotype in this phylum is a derived character that arose multiple times independently through OM loss.

The presence of a cell membrane is one of the major structural components defining life. Recent phylogenomic analyses have supported the hypothesis that the last universal common ancestor (LUCA) was likely a diderm. Yet, the mechanisms that guided outer membrane (OM) biogenesis remain unknown. Thermotogae is an early-branching phylum with a unique OM, the toga. Here, we use cryo-electron tomography to characterize the in situ cell envelope architecture of Thermotoga maritima and show that the toga is made of extended sheaths of β-barrel trimers supporting small (~200 nm) membrane patches. Lipidomic analyses identified the same major lipid species in the inner membrane (IM) and toga, including the rare to bacteria membrane-spanning ether-bound diabolic acids (DAs). Proteomic analyses revealed that the toga was composed of multiple SLH-domain containing Ompα and novel β-barrel proteins, and homology searches detected variable conservations of these proteins across the phylum. These results highlight that, in contrast to the SlpA/OmpM superfamily of proteins, Thermotoga possess a highly diverse bipartite OM-tethering system. We discuss the implications of our findings with respect to other early-branching phyla and propose that a toga-like intermediate may have facilitated monoderm-to-diderm cell envelope transitions.

L’enveloppe bactérienne est l’une des structures cellulaires les plus anciennes et les plus fondamentales. Toutefois, de nombreux aspects concernant sa diversité et son histoire évolutive sont encore inconnus. Dans cette thèse, j’ai profité du nombre croissant de génomes disponibles dans les bases de données publiques, afin de mener une analyse de phylogénomique et de génomique comparative à une large échelle évolutive. Les deux objectifs de ce travail doctoral étaient (i) d’identifier de nouvelles lignées didermes au sein des Firmicutes pour éclairer la transition monoderme/diderme, et (ii) d’élucider l’histoire évolutive de l’enveloppe cellulaire chez les bactéries et d’en déduire la nature chez le LBCA.En résumé, les résultats que j'ai obtenus au cours de cette thèse fournissent une avancée significative dans notre compréhension de la diversité et de l'évolution de l'enveloppe cellulaire, et sur l'une des transitions majeures de l'histoire des bactéries, celle entre les monodermes et les didermes
The bacterial envelope is one of the oldest and most fundamental cellular structures. Yet, many aspects of its diversity and evolutionary history are unknown. In this thesis I have taken advantage of the large available genomic data to investigate the issue through a large-scale phylogenomic and comparative genomic analyses at the level of Bacteria. The two goals of this doctoral work were (i) to identify putative new diderm lineages in the Firmicutes to illuminate the monoderm/diderm transition, and (ii) to elucidate the evolutionary history of the cell envelope in Bacteria and infer its nature in the LBCA. To sum up, the results I obtained during this thesis provide a timely and significant advancement to our understanding of the diversity and evolution of the cell envelope, and on one of the major transitions in the history of Bacteria, that between monoderms and diderms